Effect of Angiotensin receptor blockade on Plasma Osmolality and Neurohumoral Responses to High Environmental Temperature in Rats Fed a High Salt Diet

Abstract

Plasma osmolality (pOsmol) and neurohumoral signals play important roles in the pathophysiology of cardiovascular diseases. Our study investigated the effect of high environmental temperature (HET) on neurohumoral responses and pOsmol in rats fed a high salt diet (HSD), with and without angiotensin II receptor blockade (ARB), using telmisartan.  Fifty-six male 8-week old Sprague-Dawley rats (95-110g) were randomly assigned into seven groups of 8 rats. These included control rats (I) fed with 0.3% NaCl diet (normal diet, ND); salt-loaded rats (II) fed with 8% NaCl (high salt) diet; ND rats (III) exposed to HET (38.5±0.5oC ) 4 hours daily per week; rats (IV) fed with 8% NaCl diet and exposed to HET daily. Others included rats (V) fed with 8% NaCl diet and treated with telmisartan (30mg/kg); ND rats (VI) exposed to HET and treated with telmisartan; rats (VI) fed with 8% NaCl diet, exposed to HET and treated with telmisartan. Plasma angiotensin II, aldosterone, vasopressin and norepinephrine (NE) concentrations were determined by ELISA technique; pOsmol from plasma K+, Na+ and Urea. HSD combined with HET in rats synergistically increased pOsmol (P<0.001) with an associated non-synergistic rise in fluid intake (P<0.001), fluid balance (P<0.001), plasma angiotensin II (P<0.01) and aldosterone (P<0.05), NE (P<0.001) and vasopressin (P<0.05) concentrations compared to control. Telmisartan did not alter pOsmol in all the treated-rats, but normalized fluid intake levels and plasma vasopressin in the rats exposed to either HSD or HEt alone. Prolonged exposure of rats to hot environment exacerbated the effect of excess dietary salt on pOsmol, with no effect on angiotensin II-mediated neurohumoral responses

Click to view file (PDF)

References

Agbaraolorunpo, F. M., Oloyo, A. K., Anigbogu, C. N., & Sofola, O. A. (2019). Chronic exposure to high environmental temperature exacerbates sodium retention and worsens the severity of salt-induced hypertension in experimental rats via angiotensin receptor activation. Journal of African Association of Physiological Sciences, 7(2), 109–118. https://doi.org/10.4314/jaaps.v7i2.

Ali, M. A., Adem, A., Chandranath, I. S., Benedict, S., Pathan, J. Y., Nagelkerke, N., Nyberg, F., Lewis, L. K., Yandle, T. G., Nicholls, G. M., Frampton, C. M., & Kazzam, E. (2012). Responses to Dehydration in the One-Humped Camel and Effects of Blocking the Renin-Angiotensin System. PLoS ONE, 7(5). https://doi.org/10.1371/journal.pone.0037299

Allahverdi, A., Feizi, A., Takhtfooladi, M. A., & Shabani, S. (2013). Effects of high environmental temperature on plasma sodium and potassium concentrations in commercial layers. European Journal of Experimental Biology, 3(1). http://www.imedpub.com/abstract/effects-of-high-environmental-temperature-on-plasma-sodium-and-potassium-concentrations-in-commercial-layers-12110.html

Averill, D. B., Tsuchihashi, T., Khosla, M. C., and Ferrario, C. M. (1994). Losartan, nonpeptide angiotensin II-type 1 (AT1) receptor antagonist, attenuates pressor and sympathoexcitatory responses evoked by angiotensin II andL-glutamate in rostral ventrolateral medulla. Brain Research. 665(2): 245–252.

Bankir, L., Perucca, J., Norsk, P., Bouby, N., & Damgaard, M. (2017). Relationship between Sodium Intake and Water Intake: The False and the True. Annals of Nutrition and Metabolism, 70(1), 51–61. https://doi.org/10.1159/000463831

Barney, C. C., & Kuhrt, D. M. (2016). Intermittent heat exposure and thirst in rats. Physiological Reports, 4(8). https://doi.org/10.14814/phy2.12767

Baylis, P. H., & Thompson, C. J. (1988). Osmoregulation Of Vasopressin Secretion And Thirst In Health And Disease. Clinical Endocrinology, 29(5), 549–576. https://doi.org/10.1111/j.1365-2265.1988.tb03704.x

Benjamin, E. J., Blaha, M. J., Chiuve, S. E., Cushman, M., Das, S. R., Deo, R., de Ferranti, S. D., Floyd, J., Fornage, M., Gillespie, C., Isasi, C. R., Jiménez, M. C., Jordan, L. C., Judd, S. E., Lackland, D., Lichtman, J. H., Lisabeth, L., Liu, S., Longenecker, C. T., … American Heart Association Statistics Committee and Stroke Statistics Subcommittee. (2017). Heart Disease and Stroke Statistics-2017 Update: A Report From the American Heart Association. Circulation, 135(10), e146–e603.

Block, L. H., Lütold, B. E., Bolli, P., Kiowski, W., & Bühler, F. R. (1984). High salt intake blunts plasma catecholamine and renin responses to exercise: Less suppressive epinephrine in borderline essential hypertension. Journal of Cardiovascular Pharmacology, 6 Suppl 1, S95-100.

Brewster, L. M., & Seedat, Y. K. (2013). Why do hypertensive patients of African ancestry respond better to calciumblockers and diuretics than to ACE inhibitors and β-adrenergic blockers? Asystematic review. BMC Medicine, 11(1), 141. https://doi.org/10.1186/1741-7015-11-141

Campese, V. M., Romoff, M. S., Levitan, D., Saglikes, Y., Friedler, R. M., & Massry, S. G. (1982). Abnormal relationship between sodium intake and sympathetic nervous system activity in salt-sensitive patients with essential hypertension. Kidney International, 21(2), 371–378.

Cappuccio, F. P., Kerry, S. M., Micah, F. B., Plange-Rhule, J., & Eastwood, J. B. (2006). A community programme to reduce salt intake and blood pressure in Ghana [ISRCTN88789643]. BMC Public Health, 6(1), 13.

Che Muhamed, A. M., Atkins, K., Stannard, S. R., Mündel, T., & Thompson, M. W. (2016). The effects of a systematic increase in relative humidity on thermoregulatory and circulatory responses during prolonged running exercise in the heat. Temperature (Austin, Tex.), 3(3), 455–464.

Cuzzo, B., Padala, S. A., & Lappin, S. L. (2020). Vasopressin (Antidiuretic Hormone, ADH). In StatPearls. StatPearls Publishing. http://www.ncbi.nlm.nih.gov/books/NBK526069/

de Wardener, H. E., He, F. J., & MacGregor, G. A. (2004). Plasma sodium and hypertension. Kidney International, 66(6), 2454–2466.

Endo, S., Mori, T., Yoneki, Y., Nakamichi, T., Hosoya, T., Ogawa, S., Tokudome, G., Hosoya, T., Miyata, T., & Ito, S. (2009). Blockade of angiotensin II type-1 receptor increases salt sensitivity in Sprague-Dawley rats. Hypertension Research: Official Journal of the Japanese Society of Hypertension, 32(6), 513–519.

Fitzsimons, J. T. (1998). Angiotensin, thirst, and sodium appetite. Physiological Reviews, 78(3), 583–686.

Gagnon, D., Romero, S. A., Ngo, H., Poh, P. Y. S., & Crandall, C. G. (2017). Plasma hyperosmolality improves tolerance to combined heat stress and central hypovolemia in humans. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 312(3), R273–R280.

Gohlke, P., Weiss, S., Jansen, A., Wienen, W., Stangier, J., Rascher, W., Culman, J., & Unger, T. (2001). AT1 receptor antagonist telmisartan administered peripherally inhibits central responses to angiotensin II in conscious rats. The Journal of Pharmacology and Experimental Therapeutics, 298(1), 62–70.

Gonsalez, S. R., Ferrão, F. M., Souza, A. M. de, Lowe, J., Morcillo, L. da S. L., Gonsalez, S. R., Ferrão, F. M., Souza, A. M. de, Lowe, J., & Morcillo, L. da S. L. (2018). Inappropriate activity of local renin-angiotensin-aldosterone system during high salt intake: Impact on the cardio-renal axis. Brazilian Journal of Nephrology, 40(2), 170–178.

Hiroshi Nose, Gary W. Mack, Xiangrong Shi, and Ethan R. Nadel. (1994). Role of Osmolality and Plasma Volume During Rehydration in Humans. National Academies Press (US). https://www.ncbi.nlm.nih.gov/books/NBK231127/

Hughes, F., Mythen, M., & Montgomery, H. (2018). The sensitivity of the human thirst response to changes in plasma osmolality: A systematic review. Perioperative Medicine, 7(1), 1.

Johnson, A. K., & Thunhorst, R. L. (1997). The Neuroendocrinology of Thirst and Salt Appetite: Visceral Sensory Signals and Mechanisms of Central Integration. Frontiers in Neuroendocrinology, 18(3), 292–353.

Kanbay, M., Aslan, G., Afsar, B., Dagel, T., Siriopol, D., Kuwabara, M., Incir, S., Camkiran, V., Rodriguez-Iturbe, B., Lanaspa, M. A., Covic, A., & Johnson, R. J. (2018). Acute effects of salt on blood pressure are mediated by serum osmolality. Journal of Clinical Hypertension (Greenwich, Conn.), 20(10), 1447–1454.

Kaschina, E., & Unger, T. (2003). Angiotensin AT1/AT2 receptors: Regulation, signalling and function. Blood Pressure, 12(2), 70–88.

Kaya, H., Yücel, O., Ege, M. R., Zorlu, A., Yücel, H., Güneş, H., Ekmekçi, A., & Yılmaz, M. B. (2017). Plasma osmolality predicts mortality in patients with heart failure with reduced ejection fraction. Kardiologia Polska, 75(4), 316–322.

Kinsman, B. J., Simmonds, S. S., Browning, K. N., & Stocker, S. D. (2017). Organum Vasculosum of the Lamina Terminalis Detects NaCl to Elevate Sympathetic Nerve Activity and Blood Pressure. Hypertension, 69(1), 163–170.

Kosunen, K. J., Pakarinen, A. J., Kuoppasalmi, K., & Adlercreutz, H. (1976). Plasma renin activity, angiotensin II, and aldosterone during intense heat stress. Journal of Applied Physiology, 41(3), 323–327.

Leib, D. E., Zimmerman, C. A., & Knight, Z. A. (2016). Thirst. Current Biology, 26(24), R1260–R1265

Ma, X., Abboud, F. M., & Chapleau, M. W. (2001). A novel effect of angiotensin on renal sympathetic nerve activity in mice. Journal of Hypertension, 19(3 Pt 2), 609–618.

Martín-Calderón, J. L., Bustos, F., Tuesta-Reina, L. R., Varona, J. M., Caballero, L., & Solano, F. (2015). Choice of the best equation for plasma osmolality calculation: Comparison of fourteen formulae. Clinical Biochemistry, 48(7–8), 529–533.

Materson, B. J., Reda, D. J., Cushman, W. C., Massie, B. M., Freis, E. D., Kochar, M. S., Hamburger, R. J., Fye, C., Lakshman, R., and Gottdiener, J. (1993). Single-drug therapy for hypertension in men. A comparison of six antihypertensive agents with placebo. The Department of Veterans Affairs Cooperative Study Group on Antihypertensive Agents. The New England Journal of Medicine. 328(13): 914–921

Moghadamnia, M. T., Ardalan, A., Mesdaghinia, A., Keshtkar, A., Naddafi, K., & Yekaninejad, M. S. (2017). Ambient temperature and cardiovascular mortality: A systematic review and meta-analysis. PeerJ, 5, e3574.

Mozaffarian, D., Benjamin, E. J., Go, A. S., Arnett, D. K., Blaha, M. J., Cushman, M., de Ferranti, S., Després, J.-P., Fullerton, H. J., Howard, V. J., Huffman, M. D., Judd, S. E., Kissela, B. M., Lackland, D. T., Lichtman, J. H., Lisabeth, L. D., Liu, S., Mackey, R. H., Matchar, D. B., … American Heart Association Statistics Committee and Stroke Statistics Subcommittee. (2015). Heart disease and stroke statistics--2015 update: A report from the American Heart Association. Circulation, 131(4), e29-322.

Mulrow, P. J. (1999). Angiotensin II and aldosterone regulation. Regulatory Peptides, 80(1–2), 27–32.

Nadel, E. R. (1985). Recent advances in temperature regulation during exercise in humans. Federation Proceedings, 44(7), 2286–2292.

Nakamura, K., Shimizu, T., Yanagita, T., Nemoto, T., Taniuchi, K., Shimizu, S., Dimitriadis, F., Yawata, T., Higashi, Y., Ueba, T., & Saito, M. (2014). Angiotensin II acting on brain AT1 receptors induces adrenaline secretion and pressor responses in the rat. Scientific Reports, 4, 7248.

National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. (2011). Guide for the Care and Use of Laboratory Animals (8th ed.). National Academies Press (US). http://www.ncbi.nlm.nih.gov/books/NBK54050/

Nerbass, F. B., Pecoits-Filho, R., Clark, W. F., Sontrop, J. M., McIntyre, C. W., & Moist, L. (2017). Occupational Heat Stress and Kidney Health: From Farms to Factories. Kidney International Reports, 2(6), 998–1008.

Oloyo, A. K., Sofola, O. A., & Yakubu, M. A. (2016). Orchidectomy attenuates high-salt diet-induced increases in blood pressure, renovascular resistance, and hind limb vascular dysfunction: Role of testosterone. Clinical and Experimental Pharmacology & Physiology, 43(9), 825–833.

Ozsari, S. (2017). Association between Serum Osmolarity and Coronary Artery Stenosis Grade. Journal of Family Medicine, 4(6).

Ramachandran, C. D., Gholami, K., Lam, S.-K., Mustafa, M. R., & Hoe, S.-Z. (2019). Effect of high-salt diet on mean arterial pressure, renal epithelial sodium channels and aquaporin subunits expression levels in Spontaneously Hypertensive Rats. BioRxiv, 630491.

Sica, D. A. (2001). Pharmacotherapy in congestive heart failure: Angiotensin II and thirst: therapeutic considerations. Congestive Heart Failure (Greenwich, Conn.), 7(6), 325–328. https://doi.org/10.1111/j.1527-5299.2001.00274.x

Sofola, O. A., Knill, A., Hainsworth, R., & Drinkhill, M. (2002). Change in endothelial function in mesenteric arteries of Sprague-Dawley rats fed a high salt diet. The Journal of Physiology, 543(Pt 1), 255–260.

Stocker, S. D., Smith, C. A., Kimbrough, C. M., Stricker, E. M., & Sved, A. F. (2003). Elevated dietary salt suppresses renin secretion but not thirst evoked by arterial hypotension in rats. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 284(6), R1521-1528. https://doi.org/10.1152/ajpregu.00658.2002

Suckling, R. J., He, F. J., Markandu, N. D., & MacGregor, G. A. (2012). Dietary salt influences postprandial plasma sodium concentration and systolic blood pressure. Kidney International, 81(4), 407–411.

Susic, D., Varagic, J., & D Frohlich, E. (2010). Cardiovascular effects of inhibition of renin-angiotensin-aldosterone system components in hypertensive rats given salt excess. American Journal of Physiology. Heart and Circulatory Physiology, 298, H1177-81.

Szczepanska-Sadowska, E., Czarzasta, K., & Cudnoch-Jedrzejewska, A. (2018). Dysregulation of the Renin-Angiotensin System and the Vasopressinergic System Interactions in Cardiovascular Disorders. Current Hypertension Reports, 20(3), 19.

Thornton, S. N. (2018). Sodium intake, cardiovascular disease, and physiology. Nature Reviews Cardiology, 15(8), 497–497.

Toney, G. M., Chen, Q. H., Cato, M. J., & Stocker, S. D. (2003). Central osmotic regulation of sympathetic nerve activity. Acta Physiologica Scandinavica, 177(1), 43–55.

Usberti, M., Federico, S., Di Minno, G., Ungaro, B., Ardillo, G., Pecoraro, C., Cianciaruso, B., Cerbone, A. M., Cirillo, F., & Pannain, M. (1985). Effects of angiotensin II on plasma ADH, prostaglandin synthesis, and water excretion in normal humans. The American Journal of Physiology, 248(2 Pt 2), F254-259.

WHO ( 2017). Cardiovascular diseases (CVDs). Www.Who.Int/News-Room/Fact-Sheets/Detail/Cardiovascular-Diseases-(Cvds). Retrieved August 20, 2019, from https://www.who.int/news-room/fact-sheets/detail/cardiovascular-diseases-(cvds)

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Copyright (c) 2021 Nigerian Journal of Physiological Sciences